Science of the Total Environment 613–614 (2018) 635–643

Contents lists available at ScienceDirect

Science of the Total Environment

journal homepage: www.elsevier.com/locate/scitotenv

Use of food waste, fish waste and food processing waste for China's
aquaculture industry: Needs and challenge
Wing Yin Mo a, Yu Bon Man a, Ming Hung Wong a,b,c,⁎
a
Consortium on Health, Environment, Education and Research (CHEER), Department of Science and Environmental Studies, The Education University of Hong Kong, Tai Po, Hong Kong, China
b
School of Environment, Jinan University, Guangzhou, China
c
Key Laboratory for Heavy Metal Pollution Control and Reutilization, School of Environment and Energy, Peking University Shenzhen Graduate School, Shenzhen, China

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• China's aquacultural industry domi-

nates global aquaculture production
• Omnivorous and herbivorous fish are
the major species cultured in China
• Conventional ingredients could be par-
tially replaced by food waste
• Currently no laws or standards regulate
the use of food waste in fish feed

a r t i c l e i n f o a b s t r a c t

Article history: China's aquaculture industry is growing dramatically in recent years and now accounts for 60.5% of global aqua-
Received 21 February 2017 culture production. Fish protein is expected to play an important role in China's food security. Formulated feed
Received in revised form 31 August 2017 has become the main diet of farmed fish. The species farmed have been diversified, and a large amount of
Accepted 31 August 2017
‘trash fish’ is directly used as feed or is processed into fishmeal for fish feed. The use of locally available food
Available online xxxx
waste as an alternative protein source for producing fish feed has been suggested as a means of tackling the prob-
Editor: D. Barcelo lem of sourcing safe and sustainable feed. This paper reviews the feasibility of using locally available waste ma-
terials, including fish waste, okara and food waste. Although the fishmeal derived from fish waste, okara or food
Keywords: waste is less nutritious than fishmeal from whole fish or soybean meal, most fish species farmed in China, such as
Freshwater fish tilapia and various Chinese carp, grow well on diets with minimal amounts of fishmeal and 40% digestible carbo-
Marine fish hydrate. It can be concluded that food waste is suitable as a component of the diet of farmed fish. However, it will
Food waste be necessary to revise regulations on feed and feed ingredients to facilitate the use of food waste in the manufac-
Processing by-product ture of fish feed.
Fish feed
© 2017 Elsevier B.V. All rights reserved.

1. Current state of aquaculture in China

⁎ Corresponding author at: Consortium on Health, Environment, Education and
Research (CHEER), Department of Science and Environmental Studies, The Education
University of Hong Kong, Tai Po, Hong Kong, China.
E-mail address: minghwong@eduhk.hk (M.H. Wong).
The latest available statistics indicate that China has been the world's
largest producer and exporter of aquaculture products in 2015, account-
ing for 60.5% of global aquaculture production (FAO, 2017). The ratio of
fishing to aquaculture production in China was 74:26 in 1978,

http://dx.doi.org/10.1016/j.scitotenv.2017.08.321
0048-9697/© 2017 Elsevier B.V. All rights reserved.
636 W.Y. Mo et al. / Science of the Total Environment 613–614 (2018) 635–643

increasing to 30.3:69.7 in 2008 (Fishery Bureau of Department of
Agriculture, 2009). The amount of aquatic resources captured from the
environment has plateaued in the past 20 years (FAO, 2016), and it
could be expected that aquaculture production will account for a larger
proportion of the total fish supply in the future, as domestic fisheries are
over-exploited (FAO, 2016; Mallory, 2013; Villasante et al., 2013). Fish is
an important protein source and aquaculture will play an increasingly
important role in future food security.
Most freshwater fish ponds in China are polyculture ponds used for
carp and tilapia. The species commonly reared in polyculture ponds in-
clude omnivorous fish such as common carp (Cyprinus carpio), crucian
carp (Carassius spp.) and tilapia (Oreochromis spp.), herbivorous fish
such as grass carp (Ctenopharyngodon idella) and filter-feeding fish
such as silver carp (Hypophthalmichthys molitrix) and bighead carp
(Hypophthalmichthys nobilis). Table 1 lists the species farmed and their
production volumes in 2008 and 2015. China produced over 18 million
tonnes of carp and around 1.27 million tonnes of tilapia in 2015, ac-
counting for about 90% of global carp production and about 35% of glob-
al tilapia production (FAO, 2017). The data show that omnivorous and
herbivorous Chinese carp are the major species produced by China's
aquaculture industry. However, the farming practices of Chinese fish
farmers have changed. Previously, dyke pond systems that used waste
feed (various waste materials such as animal excreta, food waste or ag-
ricultural by-products) and grass (for culturing grass carp) were popu-
lar in China (Lau et al., 2003; Prein, 2002; Wong et al., 2004). Nowadays,
more and more fish farmers have adopted intensive culture methods
using formulated feed pellets (Chiu et al., 2013).
Another trend is that Chinese fish farmers have diversified the fish
species farmed. For example, the production of non-native species in
China increased from 780,000 t in 1998 to 2.5 million tonnes in 2006,
representing 5.9% and 11.7% of the total inland aquaculture production,
respectively (Liu and Li, 2010). A large quantity of tilapia (worth about
US$ 1 billion) produced in China is exported to the United States, mainly
as frozen fillets (Liu and Li, 2010). Moreover, because of the potential for
higher selling prices, an increasing number of fish farmers culture vari-
ous species of grouper, such as humpback grouper (Cromileptes
altivelis), giant grouper (Epinephelus lanceolatus), orange-spotted grou-
per (Epinephelus coioides) and hybrid grouper (Epinephelus lanceolatus
× Epinephelus fuscoguttatus) for export. Various species of grouper are
frequently consumed in luxury restaurants in Hong Kong (WWF,
2013). Furthermore, a consumer preference shift from low-value fresh-
water fish to high-value seafood has also been observed in China, driven
mainly by rapid urbanisation and higher overall levels of income in Chi-
nese society (Fish Site, 2012; Mao, 2011, 2013).
2. Problems associated with current aquaculture production in
China
The sustainability of China's aquaculture industry is being
questioned. Fishmeal is commonly used as a protein source in the diet
of farmed fish and is the most expensive ingredient in formulated fish
feed. The protein digestibility of good-quality fishmeal is very high, as
is the amino acid availability (Anderson et al., 1995). The crude protein
content of fishmeal used as feed ranges from 60% to 68% and is a good
source of essential fatty acids, minerals and trace elements (Heuzé et
al., 2015). China's aquaculture industry consumed approximately
1.4 million tonnes of fishmeal in 2015 (Mundi, 2016), and China has al-
ways been the largest importer of fishmeal from the global market (Cao

Table 1
Fish species farmed by Chinese fish farmers and their production volume.

Fish Species name Production volume in 2009** Production volume in 2015** Percentage change Diet
(tonnes) (tonnes) (%) preference

Freshwater
Grass carp Ctenopharyngodon idellus 4,081,520 5,676,235 39.1 Herbivorous
Silver carp Hypophthalmichthys molitrix 3,484,442 4,354,638 25 Filter feeder
Bighead carp Hypophthalmichthys nobilis 2,434,555 3,359,440 38 Filter feeder
Common carp Cyprinus carpio 2,462,346 3,357,962 36.4 Omnivorous
Carassius spp. Carassius spp. 2,055,478 2,912,258 41.7 Omnivorous
Nile tilapia Oreochromis niloticus 943,478 1,334,482 41.4 Omnivorous
Freshwater fishes nei Osteichthyes 489,610 601,439 22.8 Not applicable
Wuchang bream Megalobrama amblycephala 625,789 796,830 27.3 Herbivorous
Black carp Mylopharyngodon piceus 387,623 596,102 53.8 Omnivorous
Snakehead Channa argus 358,502 495,574 38.2 Carnivorous
Amur catfish Silurus asotus 325,268 450,064 38.4 Omnivorous
Blue Nile tilapia, hybrid Oreochromis aureus × O. niloticus 314,500 F 445,000 F 41.5 Omnivorous
Asian swamp eel Monopterus albus 237,034 367,547 55.1 Carnivorous
Largemouth black bass Micropterus salmoides 174,471 353,081 102.4 Carnivorous
Pond loach Misgurnus anguillicaudatus 176,405 366,186 107.6 Omnivorous
Yellow catfish Pelteobagrus fulvidraco 163,556 355,725 117.5 Omnivorous
Mandarin fish Siniperca chuatsi 235,514 298,057 26.6 Carnivorous
Channel catfish Ictalurus punctatus 223,233 264,965 18.7 Omnivorous
Pirapatinga Piaractus brachypomus 85,706 108,874 27 Herbivorous
Obscure pufferfish Takifugu obscurus 2210 5220 Carnivorous
Total 19,276,930 26,745,454 38.7
Marine fish
Marine fishes nei Osteichthyes 264,851 794,685 200 Not applicable
Large yellow croaker Larimichthys croceus 66,021 148,616 125.1 Carnivorous
Japanese seabass Lateolabrax japonicus 101,971 122,542 20.2 Carnivorous
Snubnose pompano Trachinotus blochii 66,000 F 110,000 F 66.7 Carnivorous
Groupers nei Epinephelus spp 44,155 100,006 126.5 Carnivorous
Red drum Sciaenops ocellatus 49,118 71,697 46 Carnivorous
Lefteye flounders nei Bothidae 26,672 76,837 188.1 Carnivorous
Turbot Psetta maxima 60,000 F 55,000 F −8.3 Carnivorous
Porgies, Seabreams nei Sparidae 40,253 69,795 73.4 Carnivorous
Cobia Rachycentron canadum 29,104 36,867 26.7 Carnivorous
Amberjacks nei Seriola spp 19,404 20,484 5.6 Carnivorous
Tiger pufferfish Takifugu rubripes 18,868 23,372 23.9 Carnivorous
Righteye flounders nei Pleuronectidae 11,521 8618 −25.2 Carnivorous
Total 800,148 1,643,754 105.4

**Production volume data from FAO (2017). F = FMO estimated values, nei = not elsewhere included.
 W.Y. Mo et al. / Science of the Total Environment 613–614 (2018) 635–643
Table 2
Estimated amount of protein required to grow Nile tilapia, common carp and grass carp to market size.
Fish species Marketable size Percent protein in Estimated amount of protein required Estimated fishmeal consumption References
diet to produce 1 t of fisha
Nile tilapia 400–900 g 24–34% 480–680 kg
Common carp 250–500 g 28–30% 500–600 kg
Grass carp 1.5–2.5 kg 28–30% 1120–1200 kg
a
Assuming feed conversion ratio = 2.
b
Average fishmeal inclusion rate in China for carp = 8.5%; for Nile tilapia = 2.5% (Chiu et al., 2013).
et al., 2015). China also produces a large amount of fishmeal from ‘trash
fish’ (De Silva and Turchini, 2009; Funge-Smith et al., 2005). Trash fish
are the small fish that form the low-value component of commercial
catches (Edwards et al., 2004). A large proportion of the trash fish avail-
able in China is composed of juveniles of commercially important spe-
cies, small benthic and mesopelagic fish, crustaceans and cephalopods
(Grainger et al., 2005). Unfortunately, China's capture fisheries have
been fully or over-exploited (Funge-Smith et al., 2012). In addition to
fishmeal, the production of fish feed pellets often requires various
crop products, and soybean meal is another important protein source
used in aquaculture feeds. However, the production of soybean meal re-
quires considerable arable land that could be used to grow food crops
for human consumption.
Formulated feeds have become the major diet of many important
farmed species (Olsen and Hasan, 2012). As mentioned above, carp is
the dominant group of fish cultivated in China and it has been noted
that the average inclusion rates of fishmeal for culturing Chinese carp
and Nile tilapia in China were 8.5% and 2.5%, respectively (Chiu et al.,
2013). Table 2 shows the estimated amounts of protein required to pro-
duce Nile tilapia, common carp and grass carp. Chinese carp (excluding
silver carp and bighead carp) and Nile tilapia are cultured in China in
huge volumes (10.7 and 1.2 million tonnes, respectively, in 2014)
(FAO, 2016a), so even low inclusion rates of fishmeal in fish feed can ac-
count for a substantial portion of global fishmeal demand (Chiu et al.,
2013). Furthermore, the increasing popularity of carnivorous fish cul-
ture will inevitably increase the demand for fishmeal and/or trash fish.
Carnivorous fish such as groupers require a much higher fishmeal inclu-
sion rate in their diets, up to 50% (Tacon and Metian, 2008). The estimat-
ed production volume of various grouper species in China increased by
126.5% from about 45 thousand tonnes in 2009 to 82 thousand tonnes in
2015 (FAO, 2017). Trash fish are also used by some fish farmers as a sup-
plement or directly used as feed for high-value species (Cao et al., 2015),
such as marine carnivorous fish. The annual consumption of trash fish
by China's mariculture industry is about 3 million tonnes (De Silva
and Turchini, 2009; Funge-Smith et al., 2005). However, the use of
trash fish as feed is an important cause of water quality depreciation.
Chu (2000) revealed that the amount of unconsumed feed deposited
in a group fed with pellets (24.1% ± 3.8%) was significantly lower
than in the group fed with trash fish (37.8% ± 7.8%). It was also noted
that only 8.1% of the dietary nitrogen was retained in the fish body
when trash fish were fed to areolate grouper (Epinephelus areolatus),
whereas 62% of the nitrogen was retained when moist pellets (50% pro-
tein and 20% lipid) were used as feed. Moreover, because raw fish con-
tains a high amount of moisture, aquaculture with trash fish results in a
relatively higher feed conversion ratio.
In addition to concerns about the sustainability of feed ingredients,
there are concerns about the safety of fishmeal. Fishmeal is an impor-
tant constituent in compound diets but also a major source of pollut-
ants. Fishmeal may be accidentally or deliberately contaminated with
heavy metals, persistent organic pollutants (POPs) and pesticides, and
the contamination of fishmeal appears to be a global issue. A study
showed that 55 samples of fish feed collected from the National Fish
Hatcheries of the US Fish and Wildlife Service (from October 2001 to Oc-
tober 2003) contained various POPs: all samples contained
polychlorinated biphenyl (PCBs), 39 contained chlorinated dibenzo-p-
dioxin, 24 contained polychlorinated dibenzofuran and 24 contained
637
to produce 1 t of fishb
12–17 kg Weimin (2004)
42.5–51 kg Peteri (2004), Flajšhans and Hulata (2006)
95.2–102 kg Rakocy (2005)
DDT or its metabolites (Maule et al., 2007). These POPs were also
found in several samples of salmon feed collected from fish hatcheries
in Canada, as well as other contaminants, such as arsenic, lead, copper,
zinc, fluorine and mercury (Kelly et al., 2008). It has been reported
that the fishmeal available in China may contain high levels of various
pollutants including dichlorodiphenyltrichloroethane (DDT) and mer-
cury (Cheng et al., 2014; Dickman et al., 1998; Zhou and Wong, 2000).
Poor-quality fish feeds appear to be a major source of mercury accumu-
lated in fish (Cheng et al., 2011; Lacerda et al., 2011). Moreover, trash
fish contain higher concentrations of organochlorine pesticides
(OCPs), mainly DDT or its metabolites, PCBs (Guo et al., 2009) and
total mercury and methyl mercury (Liang et al., 2011) than found in
compound feeds.
China's per capita fish consumption had grown to 33.1 kg/year in
2010 (Msangi et al., 2013). It is expected that China's population will
reach 1.41 billion by 2025 (Fu, 2015), and China is projected to account
for 38% of global consumption of fish by 2030 and to become the largest
fishmeal consumer in the coming decades (Msangi et al., 2013). It is ex-
pected that low trophic level fish such as carp and tilapia will remain the
major fish species farmed in China. To prevent the depletion of valuable
marine resources, alternatives to raw fishmeal protein sources should
be explored to satisfy the huge demand for fish while reducing the cur-
rent dependence on marine fish resources for aquaculture. Various
waste materials, such as fish waste, okara and food waste, are produced
in large quantities locally and they have potential as substitutes for con-
ventional feed ingredients.
3. Using food processing waste and food waste as fish feed
3.1. Food processing waste
3.1.1. Fish waste
Fish waste is fish tissue that is not suitable for consumption, includ-
ing bones, intestines, heads and tails, which can be used to produce
fishmeal. It has been estimated that N50% of the total fish capture is
not used as food (Kristinsson and Rasco, 2000). Fish and shrimp remains
are currently used together with trash fish, anchovies and skinnycheek
lanternfish (Benthosema pterotum) in the production of fishmeal in
China (Chiu et al., 2013). Cao et al. (2015) estimated that the annual
fish waste generated from fish processing in China could yield between
420,000 and 650,000 t of fishmeal, which is approximately 50% of the
Chinese aquaculture industry's current total demand for fishmeal. Al-
though the fishmeal derived from fish waste has a lower amount of
crude protein (58%) (Esteban et al., 2007) than high-quality fishmeal
(60% to 70%), the product is still nutritious and could be a potential
source of fishmeal for low trophic level fish. Kotzamanis et al. (2001)
noted that trout intestines leftover from from smoking fish could be a
good source of fatty acids for gilthead bream. Fish waste is indeed a
great source of minerals and fat (19% dry matter), with abundant mono-
unsaturated, palmitic and oleic acids (Esteban et al., 2007).
Because the production of Chinese carp and tilapia requires a mini-
mal amount of fishmeal, fishmeal derived from fish waste could be a
good source for culturing these species. It has been estimated that up
to 25% of fishmeal is now obtained from fish processing waste (Chiu
et al., 2013). Esteban et al. (2007) revealed that fish waste (mixed spe-
cies) collected from fishmongers in Spain had no detectable
638 W.Y. Mo et al. / Science of the Total Environment 613–614 (2018) 635–643
concentrations of arsenic, lead, mercury or cadmium. Murthy et al.
(2013) revealed that the concentrations of cadmium, lead and cop-
per present in fish meal (derived from fish heads, skin, guts, fins,
gills, livers, kidneys and scales) were 0.22 to 4.40 ppm, 4.60 to
18.20 ppm and 1.80 to 46.40 ppm, respectively, and mercury was
not detected. Kinnunen et al. (2005) found that levels of chlordane,
dieldrin, toxaphene, dichlorodiphenyldichloroethylene (DDE),
dichlorodiphenyldichloroethane (DDD), DDT and mercury in salm-
on waste from Lake Michigan and Lake Huron were below the FDA's
action levels for food fish, although the waste from fish caught in
Lake Michigan exceeded the FDA's PCB level of 2.0 ppm for food
fish. However, little is known about the concentrations of pollut-
ants in fishmeal derived from fish processing waste from China.
More information is needed to evaluate the appropriateness of
using fish waste as feed in our region.
Heat sterilisation is required to inactivate microorganisms or patho-
gens present in fish waste before further processing. However, Esteban
et al. (2007) observed that the digestibility of fish waste decreased with
temperature, and hence treatment temperatures over 105 °C are
not recommended to reduce moisture and avoid microbial growth in
the waste. As an alternative to heat treatment, low-temperature storage
can also lengthen the storage period of waste materials before
processing. However, extra investment in building infrastructure and
power consumption would be needed to utilise the waste more
efficiently.
3.1.2. Okara
Okara (also called soybean dregs or bean curd residue) is the residue
of soybean resulting from the production (soaking, blanching and boil-
ing) of tofu or soymilk. About 1.1 kg of raw okara (about 80% moisture)
is produced from processing 1 kg of soybean processed for tofu (Khare
et al., 1995). It has been estimated that about 2.8 million tonnes of
okara are produced annually by the tofu industry in China (Li et al.,
2012). Raw okara is seldom consumed by humans and it is usually
landfilled or used as animal feed. Dried okara is nutritious and it
contains about 25% to 27% crude protein and 10% crude lipids
(Mateos-Aparicio et al., 2010; O'Toole, 2016; Redondo-Cuenca et al.,
2008). Okara protein has a good essential amino acid profile and in
vitro digestibility (Chan and Ma, 1999; Ma et al., 1997). It also contains
small amounts of starch, sugars and potassium and significant levels of B
vitamins (Van der Riet et al., 1989).
Information regarding the use of okara in fish farming is limited.
El-Saidy (2011) revealed that okara could replace up to 75% of fishmeal
protein in practical diets of Nile tilapia mono-sex males without any
adverse effects on growth performance, feed utilization or the body
composition. Wong and Tang (1996) reported that common carp fed
with papain-digested okara yielded significantly better growth in
terms of weight and length gains than their counterparts without diges-
tion. In Hong Kong, raw or semi-dried okara is frequently used as feed
for carp, tilapia and grey mullet (Mugil cephalus) in polyculture ponds.
Fish farmers can obtain fresh okara from domestic soybean milk
Table 3
Quantity of food waste and its share of municipal solid waste in some major China cities.
City Year Food waste (tonnes per day)a
Hong Kong 2012 3337
Beijing 2008 726
Shanghai 2008 588
Guangzhou 2008 269
Shenzhen 2008 300
Hangzhou 2010 130
Nanjing 2008 138
Xiamen 2008 74
Guilin 2008 15
Tianjin 2006 1417b
a
Figures rounded to the nearest whole number.
b
Kitchen waste.
producers for free or at a low cost. With its cheaper price, okara could
partially replace fishmeal or soybean meal in the production of fish
feeds (Li et al., 2012; Wong and Tang, 1996).
Because of its high moisture content (about 80%), raw okara can pu-
trefy quickly if it is not preserved immediately (Taruna and Jindal, 2002;
Wachiraphansakul and Devahastin, 2005); thus, a drying process is
needed for prolonged storage. Moreover, as a derivative of soybean,
okara contains anti-nutritional factors (ANF) such as trypsin inhibitor
(Li et al., 2012). Unlike raw soybeans, however, the processes involved
in soybean milk production (soaking, blanching and boiling) can reduce
the trypsin inhibitor activity in okara by 81% when compared to raw
soybean (Wickramarathna and Arampath, 2003).
3.2. Food waste
3.2.1. Food waste as fish feed ingredients
Food waste is food that is discarded or left uneaten. In developed
countries, discarded food accounts for a relatively small amount of mu-
nicipal solid waste (MSW). Yang et al. (2012) estimated that the annual
food waste production of China is 195 million tonnes. Mian et al. (2016)
reported that food waste accounts for 55.86% of MSW in China. It has
been estimated that in total over 50 million tonnes of grain are wasted
annually at the consumer stage in China (Zheng, 2011). Decomposition
of food waste in landfills produces substantial quantities of methane – a
potent greenhouse gas with 20 times the global warming potential of
carbon dioxide (Ishigaki et al., 2002). This makes landfilling an unsuit-
able choice for disposal of food waste in China. Incineration is also not
a suitable option because the high moisture content of food waste re-
sults in low net caloric value (Liu et al., 2006; Xiao et al., 2007; Yuan
et al., 2006; Zhuang et al., 2008). Thus, instead of landfilling or inciner-
ation, food waste could be recycled. In fact, the use of food waste in an-
imal production is not a new concept.
Table 3 lists the quantity of food waste and its share in the MSW in
some Chinese cities. The data suggest that large cities in China produce
large quantities of food waste daily, accounting for N 50% of the MSW
collected (except for Hong Kong, where it is about 36%). Therefore, turn-
ing food waste into fish feed at a larger scale should be encouraged.
Information regarding the use of food waste as fish feed is limited.
Hsieh (2010) revealed that orange-spotted grouper (Epinephelus
coioides) fed diets containing 10% or 20% food waste (consisting of a
mixture of various foods, generated from a university cafeteria) showed
no significant differences in growth performance compared to the
group fed a diet with 0% food waste. Bake et al. (2013) used recycled
food waste (including soy sauce waste, leftover food from convenience
stores, food waste residues discharged during processing, hotel waste,
restaurant cooking waste, tofu waste and bread production waste) to
feed Nile tilapia and found that the groups fed diets with recycled
food waste showed no significant differences in growth performance
to the control group (fed a diet without food waste). Al-Ruqaie (2007)
studied the effects of using food waste (leftover food from bakeries
and fish markets, and hot water washed rice from restaurants) to feed
Share of municipal solid waste (%) Reference
35.97 EPD, 2016
66.19 Tai et al., 2011
71.14 Tai et al., 2011
52.00 Tai et al., 2011
51.10 Tai et al., 2011
53.00 HMSWDSC, 2010
70.59 Tai et al., 2011
74.63 Tai et al., 2011
61.31 Tai et al., 2011
56.88 TCAEEDRI, 2007
 W.Y. Mo et al. / Science of the Total Environment 613–614 (2018) 635–643
tilapia and found no significant differences in weight gain or specific
growth rate between the group fed a commercial diet and those fed
diets containing leftover food. Mo et al. (2014) revealed that food-
waste-based diets (containing 70% w/w sorted food waste meal)
contained satisfactory levels of essential amino acids, crude proteins,
crude carbohydrates, crude lipids and phosphates; such diets were suit-
able for growing low-trophic level fish, including grass carp, grey mul-
let, bighead carp and tilapia. Furthermore, the fish fed food waste-
based pellets had lower levels of contaminants (such as DDT and mercu-
ry) than those fed commercial feed pellets (Cheng et al., 2014; Cheng et
al., 2015).
These studies all suggest that food waste could be used to make fish
feed. However, these studies used food waste from specific sources and
it was sorted before use. Due to the highly heterogeneous nature of food
waste, it would be difficult to formulate feeds with acceptable nutrition-
al values without proper source separation. For example, the optimal di-
etary crude protein levels for grass carp and Nile tilapia should be 22% to
30% and 30%, respectively (Cai et al., 2005; Wang et al., 1985). Mixed
food waste generally contains around 20% crude proteins (Sayeki et
al., 2001), and therefore its protein content would still be a bit low for
low trophic level fish.
Biotransformation of food waste by microorganisms is another pos-
sible approach to enhance the crude protein content and lower fibre
content of food waste used as feed. Solid-state fermentation (SSF) is a
process in which microorganisms are grown on solid substrates in the
absence of free water (Lagemaat and Pyle, 2001). Lateef et al. (2008) re-
ported that SSF with Rhizopus stolonifer LAU 07 could significantly in-
crease the crude protein content of agro-wastes (the percentage
increase in crude protein in the wastes due to the formation of fungal
biomass ranged from 33.3% to 94.8%). Wang et al. (2010) also revealed
that SSF fermented potato pulp had significantly increased crude pro-
tein (from 3% to 5% to N 18%) and slightly increased lipid content
(from 3% to 4% to 5% to 6%), whilst the crude fibre content significantly
decreased from 40% to 50% to b 12%. Fermentation with lactic acid bac-
teria can also enhance the nutritional composition of food waste. Yang
et al. (2006) suggested that lactic acid fermentation of food waste
could break down fibre and increase water-soluble carbohydrates in
the fermentation product. Sotolu (2009) revealed that there was no sig-
nificant difference between values of SGR, PER, FCR and protein intake
between fish waste meal and fish meal based-diets at the same level
of inclusion for juveniles of African catfish (Clarias gariepinu). Goddard
et al. (2008) reported that the crude protein contents and the protein
apparent digestibility coefficient of fish processing waste meal (from a
commercial tuna and sardine cannery and fish meal plant) had no sig-
nificant differences to anchovy meal.
Mixed food waste generally contains around 60% carbohydrates, 20%
protein and 10% lipids (Sayeki et al., 2001). Liu (2014) revealed that car-
bohydrate-rich food items comprise a large proportion of food waste in
China, making food waste particularly useful to China's aquaculture in-
dustry. When fed diets containing 40% digestible starch, omnivorous
freshwater species such as tilapia and carp showed good growth perfor-
mance with normal ranges of liver size and glycogen levels (Stone,
2003). As shown in Table 1, herbivorous and omnivorous fish account
for the majority of fish cultured in China's aquaculture industry. The
high carbohydrate content of food waste could be particularly useful
for growing these fish. Nevertheless, information regarding different
methods of processing food waste as feed is relatively limited, and
more research is urgently needed.
3.2.2. Food waste-grown algae as fish feed
In addition to making pellet feeds for fish, food waste could also be
used as a nutrient source to produce microalgae. Microalgae are widely
used in fish hatcheries, either directly as a feedstuff for fish larvae or as
prey to feed other live feed such as Artemia and rotifers (Muller-Feuga,
2000). Maintaining live microalgal cultures is expensive. It has been es-
timated that investment in culturing microalgae could represent 30% of
639
a hatchery's operating cost (Coutteau and Sorgeloos, 1992), due to the
expensive culture medium used to maintain the algal culture. However,
the use of food waste hydrolysate could help to lower the cost. Pleissner
et al. (2013) reported that the fungal hydrolysate of food waste (gener-
ated from a cafeteria) could be used as a culture medium for rearing
Schizochytrium mangrovei and Chlorella pyrenoidosa, which contained
higher concentrations of protein (S. mangrovei: 259.8 mg; C.
pyrenoidosa: 130.6 mg) and lipids (S. mangrovei: 164.9 mg; C.
pyrenoidosa: 209.9 mg) than those cultured with conventional medium
(protein and lipids: S. mangrovei: 82.1 mg and 124.9 mg; C. pyrenoidosa:
69.4 mg and 48.6 mg, respectively). Lau et al. (2014) investigated the
growth of Chlorella vulgaris and reported that food waste hydrolysate
consisting of 17.9 g L− 1 glucose, 0.1 g L− 1 free amino nitrogen,
0.3 g L−1 phosphate and 4.8 mg L−1 nitrate resulted in the highest ex-
ponential growth rate in terms of biomass of 0.8 day−1.
Freeze-dried S. mangrovei could be used to enrich the arachidonic
acid (AA) and docosahexaenoic acid (DHA) contents of rotifers
(Estudillo-del Castillo et al., 2009), and live C. pyrenoidosa could be co-
fed live daphnia to larval loach (Misgurnus anguillicaudatus) to enhance
fish growth and survival when compared to the groups fed microparti-
cle diets or live daphina only (Wang et al., 2008).
Similar to fish waste and okara, pre-treatment of food waste to re-
duce moisture would be necessary before further processing because
both fresh and cooked food usually contain a higher moisture content
than uncooked food and thus favour microbial growth. Heat treatment
of the food waste at 65 °C for 20 min would be adequate to eliminate
most of the harmful microorganisms, including Enterobacteria, Clostrid-
ium and Staphylococcus aureus, with no loss of nutritional quality
(Sancho et al., 2004).
4. Regulations on the usage of waste materials as animal feed
4.1. Current regulations of food waste as animal feed
As noted above, the use of waste materials for fish production has
been practised for centuries. To the best of our knowledge, however,
food waste is not widely used in the manufacture of feed pellets. Fish
farmers in China tend to use compound pellet feeds (Chiu et al., 2013)
to maximise fish growth. Currently, the most popular application of
food waste is as swill for feeding pigs. In fact, the recycling of food
waste as swill is actively promoted and regulated by various Asian coun-
tries, including Korea, Japan, Taiwan and Thailand (Menikpura et al.,
2013), and thus far there have been no food safety issues related to
the use of food waste for feeding pigs.
In Taiwan, which started recycling food waste in 2001, about 2000 t
of food waste is recycled daily and steam-treated for use as pig swill
(Taiwan, 2014). In 2011, Japan introduced the Promotion of Utilization
of Recyclable Food Waste Act (Food Waste Recycling Law) to regulate
the collection, transport and storage of food waste and the animal feed
derived from food waste is known as ‘Ecofeed’ for growing pigs, poultry
and ruminants (Ermgassen et al., 2016). Japan successfully recycled
52.5% food waste from manufacturing, retail and catering sectors as
Table 4
Treatment methods adopted by different countries using recycled food waste as feed.
Country Treatment Reference
Japan Food waste containing meat must be Sugiura et al., 2009
heated for a minimum of 30 min at
70 °C or 3 min at 80 °C
Korea Food waste must be heat-treated for National Institute of
30 min to a core temperature of at Environmental Research,
least 80 °C 2012
Taiwan Food waste must be heated for at least Taiwan, 2014
60 min to a core temperature of 90 °C
United States Meat present in waste must be heated USDA, 2009
of America to 75 °C for 30 min
640 W.Y. Mo et al. / Science of the Total Environment 613–614 (2018) 635–643

animal feed in 2006 (MAFF, 2011). However, because household food materials or cutlery) (Chen et al., 2015). However, because there is no
waste is vulnerable to contamination by foreign objects, it is not cur- strict rule or established system to collect recyclable waste materials,
rently recycled in Japan (Sugiura et al., 2009). South Korea has also in- food waste is mixed with other waste such as plastics, papers and
troduced laws to promote the recycling of food waste as swill for pigs metals, and there is currently no strict regulation or system to collect re-
(MOAFRA, 2010; MOE, 2008), and about 42.5% of food waste was cyclable waste (Mian et al., 2016). It has been reported that the MSW
recycled as animal feed in 2006 (Kim and Kim, 2010). Growing pigs separation ratio is about 15% (Xiao et al., 2007). Food waste can only
with food waste is regulated by the Swine Health Protection Act in the be used in animal feed if it is collected separately from other waste
United States of America, but only 28 of the 50 states permit the use and is sufficiently fresh (Salemdeeb et al., 2017). Thus, with the low
of food waste as animal feed (USDA, 2016). Although the treatment waste separation ratio, the amount of recyclable food waste in China
methods vary among these countries, food waste used as animal feed could be very limited. Before processing, the materials should be prop-
must be heat-treated for sterilisation (EPA, 2013; National Institute of erly inspected and handled because hazardous contaminants can mi-
Environmental Research, 2012; USDA, 2016). Table 4 summarises the grate from printed paper bags or from the residues of cutlery or food
thermal treatment requirements of various countries. processing apparatus (Xue et al., 2010; Yang and Zhao, 2009).
The European Union has the most stringent regulations governing The safety of food waste–derived feed materials is always doubted
the use of waste as animal feed. To prevent the spread of prion diseases, by the general public. Currently in China there are laws and regulations
the use of processed animal protein, also known as meat and bone meal, relating to animal feed (including fish feed) quality and ingredients.
as animal feed has been banned in the European Union Table 5 lists some important regulations on animal feed and feed addi-
(Karapanagiotidis, 2014). Moreover, the use of waste to feed animals tives. The regulations cover a wide range of guidelines on safety, hy-
was banned due to the outbreak of foot-and-mouth disease in the UK giene requirements for the ingredients of feed and the corresponding
in 2002 (Ermgassen et al., 2016). The European Union also forbids the management measures. It is illegal to feed ruminants bovine- or
use of farmed fish by-products in finfish feeds, but they can be used in sheep-derived materials in China (MOA, 2001) and in regions such as
crustacean diets and vice versa (Newton et al., 2014). Animal producers the EU (EU Regulation (EC) No. 1069/2009, 2009), as feeding ruminants
in the European Union have had to shift from using animal waste to could transmit bovine spongiform encephalopathy (BSE). However,
using grains and/or formulated feeds. However, this has led to a large there are currently no regulations relating to turning food waste into
area of arable land being used to grow animal feed. A recent study indi- fish feed pellets. In fact, BSE does not affect pigs, poultry or fish
cated that using food waste as a primary source of swill to produce pork (Andreoletti et al., 2007). Similar to other feed products in China, feed
in Europe (which accounts for 20% of world production) could poten- derived from food waste should also comply with the Hygienic Standard
tially save 1.8 million ha of agricultural land (Ermgassen et al., 2016). for Feeds (GB 13078-2001). Chen et al. (2015) revealed that food waste
treated by fermentation, dry heating or hydrothermal treatment
4.2. Regulations of food waste as fish feed in China and its future coupled with fermentation can meet the strictest requirements of the
development Hygienic Standard for Feeds (GB 13078-2001), based on the microbial
characteristics (total aerobic plate counts, total coliform, moulds and
China's aquaculture industry consumes a huge amount of fishmeal yeast, Staphylococcus aureus, Salmonella and Listeria) and concentrations
derived from wild fish and trash fish to produce fish feed or directly of chemical contaminants (arsenic, cadmium, chromium, mercury, lead,
used as fish feed. It would be wise to make use of various waste mate- aflatoxin B1, inorganic contaminant nitrites, DDT and HCH).
rials to reduce reliance on precious marine resources and to save valu- As noted above, regulations on food waste recycling exist at the city
able agricultural land for food crops. However, there is an urgent need level only. However, unlike other countries that are recycling food
to modify the existing regulations on food waste recycling and the use waste as animal feed, China has no specialised laws to regulate the use
of food waste as fish feed. of food waste. Table 5 also lists regulations regarding the use of food
Currently there is no national law in China regarding management waste as animal feed (including fish feed) in other countries. The
strategies to regulate food waste, and regulations on food waste
recycling are at the city level only (Hu et al., 2012). Trial runs of food
Table 5
waste recycling (separated from other municipal waste) are being car- Regulations and guidelines on animal feed and feed additives: China and other countries
ried out in selected pilot cities in China (National Development and and regions.
Reform Commission, 2014). Xining (the capital of Qinghai province),
Regulations and guidelines Year issued Reference
for example, was the first city to issue regulations on food waste and amended
recycling and management (Hu et al., 2012). Currently, recycled food (if applicable)
waste is mainly used to produce compost, animal feed additives and China
biodiesel (Hu et al., 2012). Hygienical standard for feeds 2001 AQSIQ, 2001
The majority of recycled food waste is used to produce compost. Approved feed additives 2013 MOA, 2001
However, the number and the treatment capacity of composting plants Regulation on the management of 2012 State Council,
feeds and feed additives 2011
in China decreased dramatically from 134 plants and 25,461 t per day
Regulation on feed and feed additive 2014 MOA, 2014
(tpd) in 2001 to 11 plants and 5480 tpd in 2010, because the organic import registration
fraction of final compost product (about 20%) cannot meet the standard Measures for the management of production 2012 amended MOA, 2013a,
for organic fertiliser (N45%), which affects sales (Song et al., 2013). With licenses for feeds and feed additives 2013 2013b
the reduced number of treatment facilities, there is an urgent need to Single feed products directory 2008 MOA, 2008
Other countries
explore alternative methods for treating food waste other than Food waste recycling law (Japan) 2001 amended MOE, 2008
landfilling. Fortunately, treatment facilities using other treatment 2007
methods (such as anaerobic digestion or fermentation to produce ani- Wastes control act (South Korea) 2008 MOE, 2008
mal feed additives, biodiesel or biogas) are increasing (Hu et al., Control of livestock and fish feed act 2008 amended MOE, 2008
(South Korea) 2010
2012), although the number of facilities does not appear to be sufficient
Resource recycling and reuse program 2003 EPA, 2013
to handle the massive amount of food waste produced in China. (Taiwan)
Waste materials should be properly treated before their use as ingre- Waste resource recycling promotion program 2007 EPA, 2013
dients of formulated diets. The quality of raw food waste could be the (Taiwan)
most critical factor for manufacturing food waste–derived feeds because Swine health protection act garbage feeding 2009 USDA, 2009
final rules (USA)
it is difficult to remove chemical contaminants (migrated from packing
 W.Y. Mo et al. / Science of the Total Environment 613–614 (2018) 635–643
Chinese Government should revise existing regulations or enact new
regulations/national standards/accreditation systems related to the
use of waste derived materials, to provide clear guidelines for treatment
facility operators to ensure that waste materials are properly handled
and treated. For example, in South Korea, recycling food waste is regu-
lated under the Control of Livestock and Fish Feed Act Article 8. Food
waste can only be included in animal feed if it has been treated at regis-
tered feed production, of which there were 259 in 2010 (MOE, 2008). In
the United States, food waste–derived feeds must meet the regulations
and rules set by the Department of Agriculture. Meat present in waste
must be heated to 75 °C for 30 min to inactivate pathogenic organisms
(USDA, 2009) before any practical use. Despite these regulations, infor-
mation related to the use of food waste as an ingredient in fish feed is
very limited. There is an urgent need to devote more research effort to
fill the knowledge gaps on the usage and processing methods of food
waste, its economic viability and its possible negative impacts on the
environment. Moreover, a substantial research effort is needed to en-
sure the safety of fish fed with food waste, to convince the general pub-
lic and policymakers to accept food waste as fish feed.
5. Conclusions
A stable supply of fish feed is crucial to maintain food security. China
contributes significantly to global aquaculture production. Although the
fish species farmed in China are diverse, Chinese carp and tilapia will
continue to be the major aquaculture production species. A large variety
of waste materials could be utilised by the aquaculture industry to re-
duce the amount of conventional protein sources included in fish feed.
Although food waste is mainly used as pig feed, the successful cases of
using food waste as feed in South Korea, Japan and Taiwan suggest
that the idea could also be applied to fish feed production. There is an
urgent need for research to fill the knowledge gaps on the usage and
processing methods of food waste. Renewing standards and regulations
in a timely manner would also help the industry to move towards the
use of waste materials in fish feed.
Acknowledgements
Financial support from Innovative Technology Fund (Innovative
Technology Commission, Hong Kong): ITS/174/14FX, Sustainable
Fisheries Development Fund (Agriculture, Fisheries and Conservation
Department, Hong Kong): SFDF-0023, National Natural Science Founda-
tion of China (41303083), Start-up Research Grant for Newly Recruited
Assistant Professors (RG 55/2016-2017R), and The Education University
of Hong Kong, is gratefully acknowledged.
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